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Genes for Transport and Metabolism of Spermidine in Ruegeria Pomeroyi DSS-3 and Other Marine Bacteria

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Genes for Transport and Metabolism of Spermidine in Ruegeria Pomeroyi DSS-3 and Other Marine Bacteria Vol. 58: 311–321, 2010 AQUATIC MICROBIAL ECOLOGY Published online February 11 doi: 10.3354/ame01367 Aquat Microb Ecol Genes for transport and metabolism of spermidine in Ruegeria pomeroyi DSS-3 and other marine bacteria Xiaozhen Mou1,*, Shulei Sun2, Pratibha Rayapati2, Mary Ann Moran2 1Department of Biological Sciences, Kent State University, Kent, Ohio 44242, USA 2Department of Marine Sciences, University of Georgia, Athens, Georgia 30602, USA ABSTRACT: Spermidine, putrescine, and other polyamines are sources of labile carbon and nitrogen in marine environments, yet a thorough analysis of the functional genes encoding their transport and metabolism by marine bacteria has not been conducted. To begin this endeavor, we first identified genes that mediate spermidine processing in the model marine bacterium Ruegeria pomeroyi and then surveyed their abundance in other cultured and uncultured marine bacteria. R. pomeroyi cells were grown on spermidine under continuous culture conditions. Microarray-based transcriptional profiling and reverse transcription-qPCR analysis were used to identify the operon responsible for spermidine transport. Homologs from 2 of 3 known pathways for bacterial polyamine degradation were also identified in the R. pomeroyi genome and shown to be upregulated by spermidine. In an analysis of genome sequences of 109 cultured marine bacteria, homologs to polyamine transport and degradation genes were found in 55% of surveyed genomes. Likewise, analysis of marine meta- genomic data indicated that up to 32% of surface ocean bacterioplankton contain homologs for trans- port or degradation of polyamines. The degradation pathway genes puuB (γ-glutamyl-putrescine oxi- dase) and spuC (putrescine aminotransferase), which are part of the spermidine degradation pathway in R. pomeroyi, emerged as suitable targets for molecular-based studies of polyamine pro- cessing by marine bacterial communities. The frequency of genes encoding transport and catabolism of spermidine and related polyamines suggests an important role for these compounds in carbon and nitrogen budgets of marine bacterioplankton. KEY WORDS: Polyamine · Transcriptomic analysis · Microarray · Marine bacteria · Dissolved organic nitrogen Resale or republication not permitted without written consent of the publisher INTRODUCTION (Tyms 1989, Marian et al. 2000). As free constituents in seawater, however, they are only found at nM levels Spermidine and other polyamines are aliphatic (Jorgensen et al. 1993, Lee & Jorgensen 1995, Nishi- organic compounds with multiple amino groups. They bori et al. 2001, 2003), partly due to their active are synthesized by organisms across all 3 domains of turnover by marine bacteria (Höfle 1984, Lee & Jor- life, playing vital roles in diverse cellular processes gensen 1995). including nucleic acid and protein biosynthesis (Tabor Compared to extensive studies on the concentration & Tabor 1985, Higashibata et al. 2000, Kusano et al. and fate of other dissolved organic nitrogen com- 2007) and biosilica precipitation in diatom frustule for- pounds in seawater, such as dissolved free amino acids mation (Kroger et al. 2000, Sumper & Kroger 2004). In (DFAA), investigations of bacterially-mediated poly- the cytoplasm of bacteria and marine algae, intracellu- amine transformations have been rare (Höfle 1984, Lee lar soluble polyamine concentrations reach mM levels & Jorgensen 1995). Yet recent metagenomic and meta- *Email: [email protected] © Inter-Research 2010 · www.int-res.com 312 Aquat Microb Ecol 58: 311–321, 2010 transcriptomic sequencing of marine microbial com- normalized to 3 mM carbon (i.e. 0.43 mM spermidine, munities have recovered homologs of genes predicted 0.75 mM putrescine, or 1 mM serine, Table 1). Cells to be involved in spermidine and putrescine transport were grown in 200 ml chemostats at 30°C, a dilution and metabolism (Venter et al. 2004, Poretsky et al. rate of 0.125 h–1, an airflow rate of 1 ml min–1, and a 2005, Mou et al. 2008), in some cases showing evi- stirring speed of 200 rpm. Chemostat cultures were dence of differential distribution with ocean depth maintained at a constant cell density of OD600 = 0.2 for (DeLong et al. 2006). Furthermore, a recent Sargasso at least 4 retention times prior to harvesting. To harvest Sea study identified spermidine transporter proteins the cells, the outflow pumps were set to 6 ml min–1, and from SAR11 as an abundant component of the surface 9 ml of cells were directly collected in chilled tubes seawater metaproteome (Sowell et al. 2009). This containing 1 ml stop solution (5% phenol, 95% sequence-based evidence suggests that polyamines ethanol, pH = 8). Chemostat cultures were established are important substrates for heterotrophic microorgan- in quadruplicate for all 3 compounds in order to pro- isms in the ocean, with implications for the cycling of vide 4 independent replicates of each treatment for both nitrogen and carbon. microarray or qPCR analysis. In the present study, we focused on spermidine use RNA extraction, purification, and amplification. by the marine Roseobacter member Ruegeria Cells harvested from the chemostat cultures were pomeroyi DSS-3. Up to now, systematic investigations immediately centrifuged at 5000 × g (10 min) at 4°C; of spermidine transport and catabolism have been the cell pellets were then frozen at –80°C or used restricted to a few model bacteria with clinical and immediately for RNA extraction. Total RNA extraction, medical implications, such as Escherichia coli K12 mRNA purification, and mRNA amplification to amino- (Shaibe et al. 1985) and Pseudomonas aeruginosa allyl labeled antisense RNA (aa-aRNA) were per- PAO1 (Lu et al. 2002, Dasu et al. 2006). However, formed following protocols described previously Alphaproteobacteria in the Roseobacter lineage (Bürgmann et al. 2007). are prevalent in marine surface waters, where Microarray hybridization and processing. The they account for up to 20% of the total bacterio- Ruegeria pomeroyi DSS-3 whole genome microarray plankton in coastal areas and 10% in open oceans was designed on a CombiMatrix Custom Array plat- (Giovannoni & Rappe 2000). The genome sequence of form (Bürgmann et al. 2007). Along with probes for R. pomeroyi contains a number of genes that might be quality control, each array contains 12 000 probes that involved in spermidine transport (Moran et al. 2004) target 4161 out of 4348 identified genes in the and metabolism. R. pomeroyi genome (mostly 2 probes per gene; Bürg- Transcriptional profiling using whole genome mann et al. 2007). The genes that were excluded from microarray analysis (Bürgmann et al. 2007) and qPCR the array either had close homologs in the genome or was used to identify key genes for spermidine process- did not meet probe design criteria with regard to ing in Ruegeria pomeroyi, and to provide insights into hybridization temperature. transporter specificity. A comprehensive bioinformatic The aa-aRNA was fluorescently labeled and survey of polyamine-related genes in marine bacterial hybridized to the Ruegeria pomeroyi microarray as genomes and metagenomes confirmed the numerical described previously (Bürgmann et al. 2007), except abundance of polyamine transport and degradation that a non-competitive hybridization scheme was used, genes among marine bacterioplankton, and identified 2 candidate genes for Table 1. Structure and C:N ratio of 5 polyamine compounds used in the present monitoring of polyamine transforma- study and the amino acid serine tions in situ. Compound Formula C:N Chemical Structure MATERIALS AND METHODS Cadaverine C5H14N2 2.5 H2N NH2 Norspermidine C H N 2 H N NH Culture conditions. Ruegeria pome- 6 17 3 2 NH 2 royi DSS-3 cells were grown in a modi- Putrescine C4H12N2 2 H2N NH fied marine basal medium (MBM; Gon- 2 NH NH zalez et al. 2003) containing spermidine Spermidine C7H19N3 2.33 H2N 2 NH or putrescine as the sole carbon and NH Spermine C H N 2.5 H N 2 nitrogen source. Serine was also used 10 26 4 2 NH as a substrate to provide comparative O expression data for an amino acid. The Serine C3H7NO3 3 HO OH concentration of the 3 compounds was NH2 Mou et al.: Polyamine-related genes in marine bacteria 313 i.e. aa-aRNA was labeled only with a single dye (Alex- were designed using Geneious Pro software (Bio- aFluor dye 647; Invitrogen). After hybridization, the matters) and are listed in Table S1 available as supple- microarrays were scanned with an Axon GenPix 4000B mentary material at www.int-res.com/articles/suppl/ microarray scanner (Molecular Devices Corporation) a058p311_app.pdf. The designed annealing tempera- at 5 µm resolution. Images were acquired and ana- ture for each primer set ranged from 59 to 61°C. The lyzed using GenePix Pro 6.0 software (Molecular practical annealing temperature for all primer sets was Devices Corporation). The detection limits (DL) were chosen by performing a gradient PCR assay (annealing calculated based on reading of the 149 empty spots on temperature varied between 57 and 65°C) using the the array using the equation: DL = average sum of genomic DNA of Ruegeria pomeroyi as template, medians + 2×(SD). Spots with intensity below the DL and this converged at 60°C. Both aa-aRNA and non- and those identified as bad, empty, and not meeting amplified mRNA extracts that had only been treated quality assurance were excluded from further analysis. for rRNA removal (mRNA only kit; Invitrogen) were Background corrected expression data from each used as RT-qPCR templates. RNA samples were quan- array were globally normalized by trimmed means tified by spectrophotometer and were reverse tran- (2% from each side) and log2 transformed prior to scribed to cDNA with random hexamer primers at a being imported into the Acuity 4.0 software (Molecular concentration of 0.3 µg µl–1 using iScript (Bio-Rad) Devices Corporation). Analysis datasets were created according to the manufacturer’s instructions. Triplicate using the conditions (signal-to-noise ratio > 3; circular- qPCR reactions were conducted in 25 µl volumes on an ity > 80; F635% < 2; B635 CV < 50) to exclude probes iCycler IQ multicolor Real-Time PCR detection System with features close to background, saturated, with bad (Bio-Rad).
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